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Dynamical mechanism of parkinsonian beta oscillation in a heterogenous subthalamopallidal network

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Abstract

Dysfunction of basal ganglia is associated with the pathogenesis of Parkinson's disease including alteration of firing rate and excessive beta-band (13-30 Hz) synchronization activity. Neuronal heterogeneity enriches dynamics of external globus pallidus (GPe), especially showing significant differences in firing alterations under pathological state. The precise mechanism underlying these neural signatures remains elusive. To address this, we propose a subthalamopallidal network containing two classes of GPe neurons, calcium-binding protein parvalbumin (PV) and Lim homeobox (Lhx6) GPe. Our results show that Lhx6 GPe tends to rein in synchronous behavior and abnormal activity of PV GPe. Under the pathological condition, the alteration of synaptic coupling in a heterogenous pallidal network manifests itself as a direct increase of inhibitory input to PV GPe or an indirect elevation of Lhx6 GPe firing rate. These essentially enhance the inhibition of PV GPe, which results in beta-band synchronous bursting. The subthalamic nucleus (STN) is instrumental in stabilizing the spiking sequence of GPe neurons, inhibiting abnormal synchronous oscillations both in control and pathological conditions. In a dopamine-depleted state, the PV GPe-PV GPe pathway notably impacts the enhancement of beta rhythmic oscillations in STN-GPe circuit. Besides, the synaptic coupling in heterogenous pallidal and STN-GPe affect the propagation of abnormal rhythms in pallidal and subthalamopallidal networks, respectively. Our study highlights the pivotal role played by PV GPe in producing and amplifying pathological oscillatory behavior. Our results suggest that STN prevents abnormal oscillatory rhythm in GPe, providing a novel insight into the precise mechanism by which STN affects pallidal activity.

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Acknowledgements

This research was supported by the National Natural Science Foundation of China (Grants Nos. 11932003, 12272092 and 12202027).

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Authors and Affiliations

  1. Department of Dynamics and Control, Beihang University, Beijing, 100191, China

    Xiaomin Wang & Qingyun Wang

  2. School of Engineering Medicine, Beihang University, Beijing, 100191, China

    Ying Yu

  3. College of Information Science and Technology, Donghua University, Shanghai, 200051, China

    Fang Han

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  1. Xiaomin Wang
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  2. Ying Yu
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  3. Fang Han
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  4. Qingyun Wang
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All authors designed, performed the research and analyzed the data as well as wrote the paper.

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Correspondence to Fang Han or Qingyun Wang.

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Wang, X., Yu, Y., Han, F. et al. Dynamical mechanism of parkinsonian beta oscillation in a heterogenous subthalamopallidal network. Nonlinear Dyn 111, 10505–10527 (2023). https://doi.org/10.1007/s11071-023-08381-2

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